Re-examination of the Chinese record of Opisthotropis maculosa (Squamata, Natricidae), resulting in the first national record of O. haihaensis and description of a new species

A peer-reviewed open-access journa I

Zookeys 913: 141-159 (2020)

doi: 10.3897/zookeys.9 | 3.48622 RESEARCH ARTICLE #7,00Ke y

http:/ / ZOO keys -pen soft. net Launched to accelerate biodiversity research

Re-examination of the Chinese record of Opisthotropis
maculosa (Squamata, Natricidae), resulting in the first
national record of O. haihaensis and description of
a new species

Jian Wang", Zhi-Tong Lyu", Zhao-Chi Zeng', Chao-Yu Lin’, Jian-Huan Yang’,
Truong Quang Neguyen**, Minh D. Le®”®, Thomas Ziegler*'®, Ying-Yong Wang'

I State Key Laboratory of Biocontrol/The Museum of Biology, School of Life Sciences, Sun Yat-sen University,
Guangzhou 510275, China 2 Department of Zoology, Graduate School of Science, Kyoto University, Kyoto
606-8502, Japan 3 Kadoorie Conservation China, Kadoorie Farm and Botanic Garden, Lam Kam Road,
Tai Po, Hong Kong, China 4 Institute of Ecology and Biological Resources, Vietnam Academy of Science and
Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam § Graduate University of Science and Techno-
logy, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam 6 Faculty
of Environmental Sciences, VNU University of Science, Vietnam National University, Hanoi, 334 Neuyen
Trai Road, Hanoi, Vietnam 1 VNU Central Institute for Natural Resources and Environmental Studies, Hanoi
National University, 19 Le Thanh Tong, Hanoi, Vietnam 8 Department of Herpetology, American Museum
of Natural History, Central Park West at 7° Street, New York, New York 10024, USA 9 AG Zoologischer
Garten Koln, Riehler Strasse 173, D-50735 Cologne, Germany \0 Institute of Zoology, University of Cologne,
Ziilpicher Strasse 476, D-50674 Cologne, Germany

Corresponding author: Ying- Yong Wang (wangyy@mail.sysu.edu.cn)

Academic editor: R. Jadin | Received 20 November 2019 | Accepted 16 January 2020 | Published 19 February 2020
Attp://zoobank.ore/768B1F83-557A-4240-8EC2-5 9AEEC6D4BA8

Citation: Wang J, Lyu Z-T, Zeng Z-C, Lin C-Y, Yang J-H, Nguyen TQ, Le MD, Ziegler T, Wang Y-Y (2020) Re-
examination of the Chinese record of Opisthotropis maculosa (Squamata, Natricidae), resulting in the first national record
of O. haihaensis and description of a new species. ZooKeys 913: 141-159. https://doi.org/10.3897/zookeys.913.48622

Abstract

The taxonomic status of the previous record of Opisthotropis maculosa Stuart & Chuaynkern, 2007 from
Guangdong and Guangxi, southern China, is revised based on the comparison of morphological and
molecular data collected from the Chinese specimens and the holotype of O. maculosa from Thailand and
O. haihaensis Ziegler, Pham, Nguyen, Nguyen, Wang, Wang, Stuart & Le, 2019 from Vietnam. Results
reveal that the population from Shiwandashan Nature Reserve in southern Guangxi, China belongs to O.

haihaensis, and represents the first national record for China; the populations from western Guangdong

* Contributed equally as the first authors

Copyright Jian Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

142 Jian Wang et al. / ZooKeys 913: 141-159 (2020)

and southeastern Guangxi are described as a new species, Opisthotropis hungtai sp. nov. We suggest that
O. maculosa should be removed from the Chinese herpetofauna checklist. The new national record of O.
haihaensis and the description of the new species bring the total number of Opisthotropis to 13 in China.

Keywords

New national record, Opisthotropis hungtai sp. nov., southern China, taxonomy

Introduction

The genus Opisthotropis Giinther, 1872 currently comprises 23 known species, and
has spread widely throughout southern China and mainland of Southeast Asia, east-
ward to the Ryukyu Archipelago, southward to Sumatra and the Philippines (Ziegler
et al. 2008; David et al. 2011, 2015; Yang et al. 2013; Teynié et al. 2014; Wang et
al. 2017a, b). Currently, 12 species of the genus have been documented in China:
O. andersonii (Boulenger, 1888), O. cheni Zhao, 1999, O. guangxiensis Zhao, Jiang
& Huang, 1978, O. jacobi Angel & Bourret, 1933, O. kuatunensis Pope, 1928, O.
lateralis Boulenger, 1903, O. latouchii (Bouleger, 1899), O. /aui Yang, Sung & Chan,
2013, O. maculosa Stuart & Chuaynkern, 2007, O. maxwelli Boulenger, 1914, O.
shenzhenensis Wang, Guo, Liu, Lyu, Wang, Luo, Sun & Zhang, 2017, and O. zhao-
ermii Ren, Wang, Jiang, Guo & Li, 2017. O. balteata (Cope, 1895) was recently
transferred from the genus Opisthotropis to the genus Trimerodytes Cope, 1895 (Ren
et al. 2019). Most species of the genus have been well recognized on the basis of phy-
logenetic and morphological analyses from the type series or topotypic specimens,
especially in mainland China and northern Indochina (Ren et al. 2017; Wang et al.
2017; Ziegler et al. 2019). Nevertheless, the taxonomic statuses of several congeners
remain unresolved, for instance, the records of O. maculosa from Guangdong and
Guangxi in southern China (Yang et al. 2011).

Opisthotropis maculosa was originally described based on a single male specimen
from northern Thailand (Fig. 1, site 6). Subsequently, it was reported based on mor-
phological identifications in Guangdong (Fig. 1, sites 1, 2) and Guangxi (Fig. 1, sites
3, 4) in southern China (Yang et al. 2011), and northern Vietnam (Fig. 1, site 5)
(Nguyen et al. 2018). Although some minor morphological differences among Chi-
nese, Vietnamese and Thai populations were acknowledged in these publications, mo-
lecular data only became available recently, which lead to the resolution of the taxo-
nomic statuses of the Vietnamese and Chinese records of O. maculosa. The Vietnamese
record of O. maculosa was described as a distinct species, O. haihaensis Ziegler, Pham,
Nguyen, Nguyen, Wang, Wang, Stuart & Le, 2019, by comparing the molecular and
morphological data with the holotype of O. maculosa (Ziegler et al. 2019). In addi-
tion, their results also pointed out that the population of O. maculosa from Heishiding
Nature Reserve in Guangdong, southern China may represent another distinct lineage.

In the present study, the Opisthotropis specimens from Guangdong and Guangxi,
southern China previously recorded as O. maculosa, were re-examined using an integra-

New national record and a new species of Opisthotropis from China 143

VIETNAM

Hainan Island

THAILAND. >

Figure |. Collection localities of Opisthotropis hungtai sp. nov. (1 the type locality, Heishiding Nature
Reserve, Guangdong, China 2 Dawuling Forestry Station, Guangdong, China 3 Mt. Wuhuang, Guangxi,
China), O. Aaihaensis (4 Shiwandashan Nature Reserve, Guangxi, China 5 the forest near Tai Chi Village,
Quang Ninh, Vietnam) and O. maculosa (6 Phu Wua Wildlife Sanctuary, Nong Khai, Thailand), respectively.

tive taxonomic approach, by combining results from both morphological and molecular
analyses. In particular, morphological comparisons among the Chinese “O. maculosa’, the
true O. maculosa from Thailand and the recently described O. haihaensis from Vietnam
were undertaken in detail. The results demonstrate that the populations from southeast-
ern Guangxi and western Guangdong represent a distinct taxon, which is described as a
new species; the population from southern Guangxi is identified as O. haihaensis.

Material and methods

Morphometrics

Morphological examinations were performed on the holotype of Opisthotropis haihaen-
sis, specimens reported as O. maculosa by Yang et al. (2011), and several other newly
collected specimens. The collection information is given in the taxonomy accounts
below. All specimens were fixed in 10 % buffered formalin and later transferred to
70 % ethanol for preservation, and deposited in the Museum of Biology, Sun Yat-sen

144 Jian Wang et al. / ZooKeys 913: 141-159 (2020)

University (SYS), Kadoorie Farm and Botanic Garden (KFBG), and Institute of Ecol-
ogy and Biological Resources, Hanoi, Vietnam (IEBR).

Measurements followed Wang et al. (2017) and Ziegler et al. (2019) and were
taken with digital calipers to the nearest 0.1 mm. These measurements were as follows:

TL total length (from tip of snout to tip of tail);
SVL snout-vent length (from tip of snout to posterior margin of cloacal plate);
TaL tail length (from posterior margin of cloacal plate to tip of tail).

Scalation features and their abbreviations are as follows: preoculars (PrO); pos-
toculars (PtO); supralabials (SPL); infralabials (IFL); temporals (TMP); ventral scales
(V); subcaudals (SC); dorsal scale rows (DSR) were counted at one head length be-
hind head, at midbody, and at one head length before vent, respectively. Bilateral scale
counts were given as left/right.

Maxillary teeth counts (MT) were determined by subequal teeth or sockets on
right upper maxilla, and sex was determined by dissection or by the presence/absence
of everted hemipenis.

Phylogenetic analyses

The mitochondrial cytochrome 6 (CYTB) gene was used for molecular analyses. Two
new samples from Mt. Wuhuang, southeastern Guangxi and Shiwandashan Nature
Reserve, southwestern Guangxi, were included in our study. DNA extraction, PCR
amplification and sequencing followed the protocol employed by Wang et al. (2017).
In addition, 31 Opisthotropis and two outgroup sequences (following Ziegler et al.
2019) were attained from GenBank for the phylogenetic analysis (Table 1).

Amino acid sequences for the CYTB gene of all samples were first aligned using
Clustal W with default parameters. After checking the alignment to make sure that
there was no stop or error codon, the amino acid sequence dataset was transformed to
a nucleotide sequence dataset. We then applied JModelTest v2.1.2 on the nucleotide
sequence dataset under Akaike and Bayesian information criteria to determine the best-
fit nucleotide substitution model. The dataset was analyzed using maximum likelihood
(ML) in RaxmlGUI 1.3 (Silvestro and Michalak 2012) and Bayesian inference (BI) in
MrBayes 3.2 (Ronquist et al. 2012) with the GTR + I + G model. For ML analysis,
a bootstrap consensus tree inferred from 1000 replicates was used to represent the
evolutionary history of the taxa analyzed. Branches reproduced in less than 50% of
bootstrap replicates were collapsed. For BI analysis, two independent runs with four
Markov Chain Monte Carlo simulations were performed for ten million iterations and
sampled for every 1000" iteration. The first 25% of samples were discarded as burn-in.
Convergence of the Markov Chain Monte Carlo simulations was assessed using Tracer
v.1.4 (http://tree.bio.ed.ac.uk/software/tracer/). We also calculated pairwise sequence
divergence based on uncorrected p-distance using MEGA 6.06 (Tamura et al. 2013).

New national record and a new species of Opisthotropis from China 145

Table |. Localities, voucher information, and GenBank numbers for all samples used in this study.

iD Genbank No
1 Opisthotropis hungtai SYS 1000538 (Paratype) CHINA: Guangxi: Mt. Wuhuang MN890018
sp. nov.
2 Opisthotropis hungtai | SYS 1000946 (Holotype) CHINA: Guangdong: Heishiding KY594748
sp. nov. Nature Reserve
3 O. andersonii SYS 1001423 (Topotype) CHINA: Hongkong: Tai Tam KY594730
4 O. andersonii SYS 1001424 (Topotype) CHINA: Hongkong: Tai Mo Shan KY594731
5 O. cheni YBU071040 (Topotype) | CHINA: Hunan: Mangshan Nature | GQ281779
Reserve
6 O. cheni SYS 1001422 CHINA: Guangdong: Shimentai KY594741
Nature Reserve
7 O. daovantieni ROM FS39306 VIETNAM MK941140
8 O. durandi NCSM 80739 VIETNAM MK941137
9 O. guangxiensis GP746 CHINA: Guangxi GQ281776
10 O. haihaensis IEBR A.2016.34 VIETNAM: Quang Ninh: Hai Ha | MK991139
(Holotype) District
11 O. haihaensis SYS 1000537 CHINA: Guangxi: Shiwandashan MN890017
Nature Reserve _
12 MG545001_
13 MG545602
14 O. kuatunensis SYS 1001008 CHINA: Fujian: Shanghang County | KY594746
os; O. kuatunensis SYS 1001081 CHINA: Guangdong: Mt. Wutong KY594747
16 O. laui SYS 1001161 CHINA: Guangdong: Shangchuan KY594738
Island
17 O. laui SYS 1001170 CHINA: Guangdong: Shangchuan KY594739
Island
18 O. lateralis SYS 1000951 CHINA: Guangdong: Heishiding KY594743
Nature Reserve
19 KY594744
20 GQ281782
21 O. latouchii SYS 1000670 (Topotype) CHINA: Fujian: Mt. Wuyi KY594742
22; O. latouchii GP647 CHINA: Fujian GQ281783
23 O. maculosa FMNH 265798 THAILAND: Nong Khai: Phu Wua | MK991138
(Holotype) Wildlife Sanctuary
24 O. maxwelli SYS 1000841 CHINA: Guangdong: Nan’ao Island | KY594736
25 O. maxwelli SYS 1001053 CHINA: Fujian: Huboliao Nature KY594737
Reserve
26 O. shenzhenensis SYS 1001018 (Holotype) | CHINA: Guangdong: Mt. Wutong KY594727
27 O. shenzhenensis SYS 1001021 (Paratype) |CHINA: Guangdong: Mt. Sanzhoutian] KY594728
28 KY594729
29 O. voquyi ZFMK 100819 (Paratype) | VIETNAM: Bac Giang: Tay Yen Tu | MG451049
Nature Reserve
30 O. voquyi ZFMK 100820 (Paratype) | VIETNAM: Bac Giang: Tay Yen Tu | MG451050
Nature Reserve
31 O. zhaoermii CIB109998 (Paratype) CHINA: Hunan: Guzhang County | MG012799
32 O. zhaoermii CIB109999 (Holotype) CHINA: Hunan: Guzhang County | MG012800
33 O. zhaoermii CIB110000 (Paratype) CHINA: Hunan: Guzhang County | MG012801
Outgroups
34 Aspidura RS-M SRI LANKA: Nuwara Eliya KC347455
drummondhayi

35 Aspidura trachyprocta RS-134 SRI LANKA: Nuwara Eliya KC347458

146 Jian Wang et al. / ZooKeys 913: 141-159 (2020)

SYS 1000538
us | Opisthotropis sp. nov.

G #/99 SYS 1000946
IEBR .A.2016.34
| he | O. haihaensis
-/-| SYS 1000537

| am { ZEMK 100819
| O. voquyi
| 0.99/95 ZFMK 100820
F «x [ IEBR 4329 =

4 | O. jacobi

ZFMK 100818
CIB 110000

o/s

cis 109999 | O. zhaoermii
0.97/93 CIB 109998

ain | SYS 1001422
+ /% O. cheni
-/- GP 383

SYS 1000670
Ae fe O. latouchii
GP 647
0.93/- a/ep SYS 1001081

| O. kuatunensis
E SYS 1001008

FMNH 265798 | O. maculosa

w/e SYS 1001161 ;
O. laui
SYS 1001170
SYS 1001032
#/®
isp -/- SYS 1001021 | O. shenzhenensis
i = aie Na

/83 SYS 1001018
wnt SYS 1001424 7
ees O. andersonii

D ee SYS 1001423
+/99 jaf SYS 1001053 ;
— ali . maxwelli
ag SYS 1000841
af SYS 1001080
[x
sys 1000951 | O. lateralis
Cc GP 646
B ROM FS39306 | O. daovantieni
A NCSM 80739 | O. durandi

GP 746 | O. guangxiensis
RS-134 Aspidura trachyprocta
RS-M Aspidura drummondhayi

Figure 2. Bayesian Inference and Maximum Likelihood phylogenies. The Bayesian posterior probabili-
ties (BPP) > 0.90 and the bootstrap supports for Maximum Likelihood analysis (BS) > 80 were retained.

Results

The CYTB nucleotide sequence matrix contained 1059 characters without insertion-
deletions. The MP and BI analyses produced essentially identical topologies, which
were integrated in Fig. 2. Major nodes of the tree were sufficiently supported, with
Bayesian posterior probabilities (BPP) > 0.90 and bootstrap supports (BS) for maxi-
mum likelihood analysis > 80. Uncorrected p-distances among Opisthotropis species

based on the CYTB gene are shown in Table 2.

147

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148 Jian Wang et al. / ZooKeys 913: 141-159 (2020)

In our phylogenetic tree, all samples of the genus Opisthotropis clustered in a
monophyletic group with high nodal supports (BPP 1.00 and BS 100), and can be
divided into seven clades, although the relationships among these clades were unre-
solved. Opisthotropis daovantieni Orlov, Darevsky & Murphy, 1998, O. durandi Tey-
nié, Lottier, David, Nguyen & Vogel, 2014 and O. guangxiensis formed three mono-
typic clades, respectively. Opisthotropis andersonii, O. lateralis, O. laui, O. maxwelli,
and O. shenzhenensis were grouped in clade D (BPP 1.00 and BS 99). Clade E (BPP
0.93) contained O. cheni, O. kuatunensis, O. latouchii, the true O. maculosa, and O.
zhaoermii. The sister species O. jacobi and O. voguyi Ziegler, David, Ziegler, Pham,
Nguyen & Le, 2018 constituted clade F (BPP 0.99 and BS 95).

Within clade G (BPP 1.00 and BS 99), the Opisthotropis sample (SYS 1000537)
from Shiwandashan Nature Reserve, southern Guangxi, was placed with the holotype
of O. haihaensis from northeastern Vietnam, with high node support values (BPP 1.00
and BS 100) and moderate genetic distance (p-distance 4.6%). The detailed morpho-
logical examination suggests that they represent individuals of the same species. ‘Thus,
we herein revise the identification of the specimen as O. haihaensis, and report it as a
new national record for China.

Besides, the Opisthotropis samples from Mt. Wuhuang, southeastern Guangxi and
Heishiding Nature Reserve, western Guangdong, were reconstructed as a monophylet-
ic clade with strong nodal supports (BPP 1.00 and BS 100) and small genetic distance
(p-distance 2.8%). The populations should be considered as a distinct taxon, which
is sister to O. haihaensis. These specimens show almost no morphological differences
from those collected at Dawuling Forestry Station, western Guangdong, which is lo-
cated in the same mountain belt as Heishiding Nature Reserve. Therefore, we describe
these specimens as a new species, Opisthotropis hungtai sp. nov.

Taxonomy accounts

Opisthotropis haihaensis Ziegler, Pham, Nguyen, Nguyen, Wang, Wang, Stuart &
Le, 2019
Figures 3, 5A

Chresonymy. Opisthotropis maculosa Stuart & Chuaynkern, 2007: Yang et al. (2011)
(part); Nguyen et al. (2018).

Holotype. IEBR A.2016.34 [Field No. QN 2016.91], adult female, from the for-
est near Tai Chi Village, Quang Son Commune, Hai Ha District, Quang Ninh Prov-
ince, 950 m asl., Vietnam [exact locality and coordinates not provided owing to threat
from collection for the pet trade (Ziegler et al. 2019)], collected by Cuong The Pham
and ‘Tan Van Nguyen on 9 May 2016.

Specimens examined (N = 1). SYS 2000537, adult female, collected by Qing Du
and Jian-Huan Yang on 10 July 2009 from Shiwandashan Nature Reserve [exact coor-
dinates not provided owing to threat from collection for the pet trade], Shangsi Coun-

ty, Qinzhou City, Guangxi Zhuang Autonomous Region, 493 m a.s.l., PR. China.

New national record and a new species of Opisthotropis from China 149

5mm 5mm

Figure 3. Morphological features of Opisthotropis haihaensis (SYS 1000537) from Shiwandashan Nature
Reserve, Guangxi, China. A Habitus view B=-D close-up of head scales. Photos by Jian Wang.

Etymology. According to the original description, the specific name “haihaensis”
refers to the type locality of this species, Haiha District (Quang Ninh Province) in
Vietnam. As this species is currently reported in China, we suggest its Chinese name
“Hai He Hou Leng She (JAH"] fa #2)”, derived from its scientific name.

Variation. Measurements, scalation and body proportions of the two speci-
mens are listed in Table 3. The specimen from China conforms to the holotype
from Vietnam except for: (1) a shorter body size: snout-vent length 391.3 mm, tail
length 108.9 mm (vs. SVL 396 mm, Tal 113 mm in the holotype); (2) a higher
number of postoculars: PtO 2 (vs. PtO 1 in the holotype); (3) a lower number of
maxillary teeth: MT 22 (vs. MT 24 in the holotype); (4) a lower number of ven-
trals: V 164+2 (vs. V 169+2 in the holotype); (5) a lower number of subcaudals: SC
75 (vs. SC 79 in the holotype); and (6) tail scales indistinctly keeled (vs. tail scales
smooth in the holotype).

Revision of original diagnosis. Opisthotropis haihaensis is characterized by the
combination of the following characters: (1) TL 500.2-509 mm in adult females,
(2) tail relatively long, TaL/TL 0.22, (3) internasal not in contact with loreal, prefrontal
not touching supraocular, frontal touching preocular, (4) one preocular, one or two
postocular(s), (5) temporals 1+1, (6) supralabials eight, fourth and fifth in contact with
eye, (6) 22—24 maxillary teeth, (7) anterior pair of chin shields longer than posterior

Jian Wang et al. / ZooKeys 913: 141-159 (2020)

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New national record and a new species of Opisthotropis from China 151

pair; (8) ventrals 164-169 (+ 2 preventrals), (9) subcaudals 75—79, (9) nasal cleft point-
ing to the first supralabial, (10) body scales in 15-15-15 rows, (11) body scales smooth,
tail scales smooth or indistinctly keeled, (12) chin shields yellow with brownish black
mottling, and (13) body and tail dorsum dark, each with a light yellow spot per scale.

Coloration in life (SYS 1000537). Eye black; scales on dorsal surface of head
glossy black with scattered yellow flecking; chin shields yellow with brownish black
mottling; body and tail glossy black with iridescence above, with single yellow spot on
each scale, yellow spots becoming larger on sides of body; ventrals yellow with brown-
ish black lateral margins and scattered brown flecks; subcaudals yellow with brownish
black anterior and lateral margins in both specimens.

Coloration in preservation (SYS 1000537). Ground color of upper head and
body surface dark brown, that of venter yellowish-beige. Dorsal scales each with light
blotch in the center. Dorsal tail scales likewise with light central blotches. Dorsal head
surface in part with indistinct light mottling. Anterior supralabials with large light
mottling. Infralabials, chin shields and smaller throat scales anterior to ventrals yel-
lowish-beige with dark brown mottling per scale. Belly with few, scattered dark flecks
on sides. Outermost edges of light ventrals brown. Ground color of subcaudals brown
with transversally enlarged light blotches at each scale end.

Distribution and habits. Opisthotropis haihaensis is currently known from its type
locality, the forest near Tai Chi Village (ca 950 m a.s.l.), Quang Ninh, northern Vi-
etnam, and Shiwandashan Nature Reserve (ca 500 m a.s.l.), southwestern Guangxi,
southern China. ‘The straight-line distance between the two localities is approximately
150 kilometers, indicating that the distribution area of this species is the mountain
region on the border between China and Vietnam.

The holotype was found at night in a small rocky stream at 21:30h. The surround-
ing habitat was secondary evergreen forest consisting of small hardwoods, bamboo,
and shrubs. The air temperature was 24—29 °C and the relative humidity was 65-88%.
The holotype revealed to be an adult female, as dissection showed up to 16.5 mm long
eggs and the oviducts were folded, indicating that eggs had already been laid (Ziegler
et al. 2019). Besides, the other specimen, SYS 1000537, was collected from a rocky
stream (about 8 m wide and 0.3 m deep at the collecting site) running through well-
preserved, dense deciduous forests. ‘The collected individual was spotted swimming at
night and swiftly hiding under stones when disturbed.

Opisthotropis hungtai sp. nov.
hetp://zoobank.org/AOFC2C8F-866B-4D8 1-9237-1E42942711AA
Figures 4, 5B, 6

Chresonymy. Opisthotropis maculosa Stuart & Chuaynkern, 2007: Yang et al. (2011)
(part); Wang et al. (2017a), Ren et al. (2019).
Holotype. SYS 1000946, adult male, collected by Jian Zhao on 2 September

2014 from Heishiding Nature Reserve [exact coordinates not provided owing to threat

kp? Jian Wang et al. / ZooKeys 913: 141-159 (2020)

ed Sen ese? Ee Pa oe
Figure 4. Morphological features of the adult male holotype SYS 100946 of Opisthotropis hungtai sp.

noy. A Habitus view in life B habitus view in preservative C close-up of mid-dorsal body D-E close-up

of head scales. Photos by Jian Zhao and Jian Wang.

from collection for the pet trade, same as paratypes], Fengkai County, Zhaoqing City,
Guangdong Province, 300 m a.s.1., PR. China.

Paratypes (N = 7). Adult female SYS r001350 collected by Zhi-Tong Lyu on 15
August 2015, adult female SYS 1000720 collected by Ying-Yong Wang on 28 June
2012, and adult female SYS 1001525 collected by Zhi-Tong Lyu and Ying-Yong Wang
on 1 July 2016, from the same locality as the holotype. Adult male KFBG 2002.01
collected by Zhi Xiao on 2 July 2002, adult male SYS 1002017 collected by Jian Wang
on 14 June 2018, and adult male SYS 2001515 collected by Jian Wang on 8 July 2017,
all from Dawuling Forestry Station, Xinyi City, Maoming City, Guangdong Province,
ca 1150 mas.l., PR. China. Adult male SYS 2000538, collected by Qing Du and
Runlin Li on 14 July 2009 from Mt. Wuhuang, Pubei County, Qinzhou City, Guangxi
Zhuang Autonomous Region, ca 360 ma.s.l., PR. China.

Etymology. The species name “hungtai” refers to Professor Hung-Ta Chang
(=Hong-Da Zhang, TKEIA), an outstanding botanist, who established the Tropical
and Subtropical Forest Ecosystem Experimental Center in Heishiding Nature Reserve,
promoting the development of ecological research in southern China. We suggest the
English common name Hung-Ta Chang’s mountain Keelback and the Chinese name
Zhang Shi Hou Leng She (Kk Ja tee).

Diagnosis. Opisthotropis hungtai sp. nov. is characterized by the following combination
of characters: (1) TL 464.3-501.2 mm in adult males, 393.2—511 mm in females, (2) tail
moderate, TaL/TL 0.20-0.26 in males, 0.19—0.22 in females, (3) internasal not in contact
with loreal, prefrontal not touching supraocular, frontal touching preocular, (4) one pre-

New national record and a new species of Opisthotropis from China tes)

ocular, one or two postocular(s), (5) temporals 1+1, (6) supralabials seven, the fourth and
fifth in contact with eye; (6) maxillary teeth 16-18, (7) anterior pair of chin shields longer
than or equal to posterior pair; (8) ventrals 170-189 (+ 2 preventrals) in males, 168-175
(+ 2 preventrals) in females, (9) subcaudals 76-98 in males, 69-84 in females, (9) nasal
cleft pointing to the second supralabial, (10) body scale in 15—15—15 rows, (11) body scales
smooth, tail scales smooth or indistinctly keeled, (12) chin shields yellow with brownish
black mottling, and (13) body and tail dorsum dark, each with a light spot per scale.
Comparisons. Opisthotropis hungtai sp. nov. is compared with O. maculosa and O.
haihaensis, which share a very similar appearance. Measurements, scalation and body
proportions of O. haihaensis and Opisthotropis hungtai sp. nov. are listed in Table 3.
Opisthotropis hungtai sp. nov. differs from O. maculosa by prefrontal not touching
supraocular (vs. prefrontal touching supraocular in O. maculosa), by frontal touch-
ing preocular (vs. frontal not touching preocular in O. maculosa), by fourth and fifth
supralabials in contact with eye (vs. fourth supralabial in contact with eye in O. macu-
losa), by anterior pair of chin shields longer than or equal to posterior pair (vs. anterior
pair of chin shields shorter than posterior pair in O. maculosa), by a higher number of
subcaudals, 76-98 in males (vs. 67 in the single male holotype of O. maculosa), and
by chin shields yellow with brownish black mottling (vs. immaculate in O. maculosa).
Opisthotropis hungtai sp. nov. differs from O. haihaensis by having seven suprala-
bials, the second last one significantly enlarged, narrow and long, significantly wider
than high (vs. eight supralabials, the second last one slightly enlarged, slightly wider
than high in O. haihaensis) (Fig. 5), and MT 16-18 (vs. MT 22-24 in O. haihaensis).
Description of holotype. Body cylindrical, slender, round to oval in cross section; TL
501.2 mm (SVL 401.6 mm, TaL 99.6 mm); tail thin and pointed, TaL 20% of TL; head
small, indistinct from neck; right upper maxilla with 16 subequal teeth or sockets, teeth
small, curved, without diastema; rostral nearly flattened, small, slightly less than twice as
broad as deep, barely visible from above; two internasals, crescent-shaped, in contact with
each other medially behind the rostral, not in contact with loreal, posteriorly in contact
with prefrontal; a single prefrontal, in contact with loreal and preocular laterally, with
frontal posteriorly, not in contact with supraocular; a single frontal, hexagonal, in contact
with supraocular laterally, with two parietals posteriorly; parietals large, in contact with
each other medially; nasal directed dorsally, polygonal, in contact with first and second
supralabials ventrally, with loreal and prefrontal posteriorly, with internasal dorsally, with
rostral anteriorly; nostril horizontally oval, in the upper part of nasal; a short vertical cleft
below the nostril and dividing nasal into anterior and posterior parts, pointing to middle
of upper edge of second supralabial; a single loreal, trapezoid, not entering the orbit, in
contact with second and third supralabials laterally; a single supraocular, much longer
than wide, obliquely set; a single preocular, higher than wide, in contact with frontal; a
single postocular; a single anterior temporal, significantly elongate, in broad contact with
the elongated sixth supralabial; a single posterior temporal, pentagonal; supralabials 7/7,
the sixth one significantly elongate, the last one much shorter than the adjacent preced-
ing supralabial; fourth and fifth supralabials entering orbit; infralabials 7/7, the first one
in contact with its fellow behind the mental; two pairs of chin shields; anterior chin

154 Jian Wang et al. / ZooKeys 913: 141-159 (2020)

B. Opisthotropis hungtai sp. nov.(SYS rO00946)

Figure 5. Comparisons of head scalation of Opisthotropis haihaensis and Opisthotropis hungtai sp. nov.
Line illustration by Zhi-Tong Lyu.

shields larger, in contact with each other medially, and in contact with the first four in-
fralabials on both sides; posterior chin shields smaller, in contact with each other; dorsal
scales in 15-15-15 rows; dorsal scales of body smooth throughout; dorsal scales of tail
weakly keeled; ventrals 170; cloacal plate divided; subcaudals 76, paired.

Coloration of holotype in life. Eye black; scales on dorsal surface of head glossy
dark brown with scattered yellow flecking; chin shields yellow with brownish black
mottling at each margin; body and tail glossy dark brown with single yellow spot
on each scale, yellow spots becoming larger on sides of body; ventrals yellow with
brownish black lateral margins and few scattered brown flecks; subcaudals yellow with
brownish black anterior and lateral margins.

Coloration of holotype in preservative. Ground color of upper head and body
surface dark brown (Fig. 4B), that of venter yellowish-beige. Dorsal scales each with

New national record and a new species of Opisthotropis from China 155

Figure 6. Morphological features of the adult female paratypes of Opisthotropis hungtai sp. nov. from

Dawuling Forestry Station, Guangdong, China. A, B Habitus view and close-up of mid-dorsal body of
SYS 1001515 C=E habitus view and close-up of head scales of SYS r002017. Photos by Jian Wang.

light yellow blotch in the center. Dorsal blotches almost equal in size. Blotches becom-
ing wider towards body sides; largest at outermost dorsal scale row, where the light
blotches stretch towards the posterior scale end. Dorsal tail scales likewise with light
central blotches. Dorsal head surface in part with indistinct light mottling that becomes
more obvious on temporals. All supralabials with a light blotch. Infralabials, chin shields
and smaller throat scales anterior to ventrals light yellow with brown mottling/blotches
per scale. Belly with few, scattered dark flecks. Outermost edges of light ventrals brown.
Ground color of subcaudals light yellow with black anterior and lateral margins.
Variations. Measurements, body proportions and scale counts are listed in Table
3. All paratype specimens are very similar to the holotype in appearance (Fig. 6) ex-
cept: more maxillary teeth, ventrals and subcaudals, and relatively longer tail length
in specimens KFBG 2002.01, SYS 1001515, 2017 from Dawuling Forestry Station
and SYS 1000538 from Mt. Wuhuang; in the three female specimens from the same

156 Jian Wang et al. / ZooKeys 913: 141-159 (2020)

locality (Heishiding Nature Reserve) as the holotype, there are 17 maxillary teeth (vs.
16 maxillary teeth) and fewer subcaudals, 56 (broken tail) in SYS r000720, 69 in SYS
1001350, 70 in SYS 1001525 (vs. 76 in the male holotype).

Distribution and habits. Opisthotropis hungtai sp. nov. is currently known from
Heishiding Nature Reserve (ca 300 m a.s.l.) and Dawuling Forestry Station (ca 900 m
a.s.l.) in western Guangdong, and Mt. Wuhuang (ca 500 ma.s.l.) in southeastern Guangxi.

The specimen from Mt. Wuhuang was collected in a rocky stream. Besides, speci-
mens from Heishiding Nature Reserve were found in pelitic gutterways along the dirt
path, and specimens from Dawuling Forestry Station were collected in a pelitic stream.
The collection sites were all surrounded by well-preserved, dense deciduous forest.

Discussion

As a representative snake group of the Oriental Realm, the mountain Keelback genus
Opisthotropis receives more attention for its important role as an environmental indi-
cator. Mountain Keelbacks are generally adapted to rocky forest streams (Wang et al.
2017a, b). However, species delimitations in this genus are still poorly resolved. The
true diversity of Opisthotropis was underestimated, which is fatal for appropriate con-
servation of these habitat specialists. According to the integrative taxonomic approach,
i.e, combining detailed morphological and molecular analyses, used in this study,
the record of O. maculosa should be removed from the Chinese herpetofauna. So far,
the true O. maculosa is restricted to northern Thailand, with only a single individual
recorded. Opisthotropis haihaensis occurs in the mountain regions along the China-
Vietnam border with only two female specimens recorded up to now, and O. hungtai
is known only from the hilly regions between Guangxi and Guangdong of southern
China. Extended surveys are urgently needed over the broad region from southern
China to northern Thailand to investigate the distribution and the population status of
these three species. Due to their beautiful color patterns, the snakes are in high demand
in the animal trade market (Ziegler et al. 2019), and they must be evaluated for inclu-
sion in one of the conservation categories in the IUCN Red List of Threatened Species.

The discovery of Opisthotropis hungtai sp. nov. brings the total number of species
of Opisthotropis to 24. Nevertheless, with regard to recent phylogenetic results (Ren et
al. 2017; Wang et al. 2017; Ziegler et al. 2019; this study), the relationships of clades
within this genus still remain largely unresolved. As the mitochondrial CYTB gene
is unable to generate significant support values, further work employing multilocus
nuclear-gene and matrilineal mtDNA genealogy is recommended to decipher this puz-
zle. In addition, the similar appearance of O. maculosa, O. haihaensis and O. hungtai,
together with their distant genetic divergence, indicates cryptic speciation in the genus
Opisthotropis. The non-monophyletic relationships between O. maculosa and the clade
composed of O. hungtai and O. haihaensis in our phylogenetic tree indicate that identi-
cal or similar phenotypes have evolved independently.

New national record and a new species of Opisthotropis from China 157

Key to the species included in Opisthotropis maculosa sensu lato

1 Prefrontal touching supraocular eels eeseeseeeseeseeseceseeseeeeees O. maculosa
— Prefrontal ne@t-tOuchinie SMP cular: ....,.1s0) Shewwssmbasetoncnibseapedeiis rbabieu yedeeds gas 2
2 Supralabials eight, the second last one significantly enlarged; maxillary teeth
PI Ps OR AOR ONE POL OE OCR eA Rn Te O. haihaensis
— Supralabials seven, the second last one slightly enlarged; maxillary teeth
16 Gaol Secon eames Airs ayer, a et et, ref Rene LIRTE. O. hungtai
Acknowledgements

We would like to thank Can-Rong Lin, Qing Du, Run-Lin Li, Jian Zhao, and Zhi
Xiao, for their help in the field. This work was supported by the Scientific Expedi-
tion of Biological Resources of Yunkai Mountains in Guangdong Province (No.
2018B030320001) and the Specimen Platform of Ministry of Science and Technol-
ogy, PR. China, teaching specimens sub-platform (No.2005DKA21403JK).

References

Angel F, Bourret R (1933) Sur une petite collection de serpents du Tonkin. Descriptions
d’espéces nouvelles. Bulletin de la Société Zoologique de France 58(3—4): 129-140.

Boulenger GA (1888) Description of two new snakes from Hong Kong and note on the denti-
tion of Hydrophis viperina. Annals and Magazine of Natural History 2(6): 43-45. https://
doi.org/10.1080/00222938809460874

Boulenger GA (1899) On a collection of reptiles and batrachians made by Mr. J.D. La Touche
in N.W. Fokien, China. Proceedings of the Zoological Society of London 1899: 159-172.
[pls. 16-19]

Boulenger GA (1903) Descriptions of new snakes in the collection of the British Muse-
um. Annals and Magazine of Natural History, Series 7, 12(69): 350-354. https://doi.
org/10.1080/00222930308678866

Boulenger GA (1914) Descriptions of new species of snakes in the collection of the British
Museum. Annals and Magazine of Natural History, Series 8, 14(84): 482—485. https://doi.
org/10.1080/00222931408693606

David P, Pauwels OSG, Nguyen TQ, Vogel G (2015) On the taxonomic status of the
Thai endemic freshwater snake Parahelicops boonsongi, with the erection of a new ge-
nus (Squamata: Natricidae). Zootaxa 3948(2): 203-217. https://doi.org/10.11646/
zootaxa.3948.2.3

David P, Pham TC, Nguyen QT, Ziegler T (2011) A new species of the genus Opisthotropis
Giinther, 1872 (Squamata: Natricidae) from the highlands of Kon Tum Province, Viet-
nam. Zootaxa 2758: 43—56. https://doi.org/10.11646/zootaxa.2758.1.3

158 Jian Wang et al. / ZooKeys 913: 141-159 (2020)

Giinther ACLG (1872) Seventh account of new species of snakes in the collection of the
British Museum. Annals and Magazine of Natural History 9(4): 13-37. https://doi.
org/10.1080/002229372011951771

Pope CH (1928) Seven new reptiles from Fukien Province, China. American Museum Novi-
tates 320: 1-6.

Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Héhna S, Larget B, Liu L,
Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic infer-
ence and model choice across a large model space. Systematic Biology 61(3): 539-542.
https://doi.org/10.1093/sysbio/sys029

Ren JL, Wang K, Jiang K, Guo P, Li JT (2017) A new species of the Southeast Asian genus
Opisthotropis (Serpentes: Colubridae: Natricinae) from western Hunan, China. Zoological
Research 38(5): 251-263.

Ren JL, Wang K, Guo P, Wang YY, Nguyen TT, Li JT (2019) On the generic taxonomy of
Opisthotropis balteata (Cope, 1985) (Squamata: Colubridae: Natricinae): taxonomic revi-
sion of two natricine genera. Asian Herpetological Research 10(2): 105-128.

Stuart BL, Chuaynkern Y (2007) A new Opisthotropis (Serpentes: Colubridae: Natricinae) from
Northeastern Thailand. Current Herpetology 26(1): 35—40. https://doi.org/10.3105/1345-
5834(2007)26[35:ANOSCN]2.0.CO;2

Silvestro D, Michalak I (2012) RaxmlGUI: a graphical front-end for RAxML. Organisms Di-
versity and Evolution 12(4): 335-337. https://doi.org/10.1007/s13127-011-0056-0

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGAG6: molecular evolution-
ary genetics analysis, version 6.0. Molecular Biology and Evolution 30(12): 2725-2729.
https://doi.org/10.1093/molbev/mst197

Teynié A, Lottier A, David P, Nguyen TQ, Vogel G (2014) A new species of the genus Opisthotro-
pis Giinther, 1872 from northern Laos (Squamata: Natricidae). Zootaxa 3774(2): 165—
182. https://doi.org/10.11646/zootaxa.3774.2.4

Wang YY, Guo Q, Liu ZY, Lyu ZT, Wang J, Luo L, Sun YJ, Zhang YW (2017a) Revisions of
two poorly known species of Opisthotropis Giinther, 1872 (Squamata: Colubridae: Natri-
cinae) with description of a new species from China. Zootaxa 4247(4): 391-412. https://
doi.org/10.11646/zootaxa.4247.4.3

Wang J, Lyu ZT, Zeng ZC, Liu ZY, Wang YY (2017b) Re-description of Opisthotropis laui
Yang, Sung and Chan, 2013 (Squamata: Natricidae). Asian Herpetological Research 8(1):
70-74. https://doi.org/10.16373/j.cnki.ahr. 160032

Yang JH, Sung YH, Chan BPL (2013) A new species of the genus Opisthotropis Giinther, 1872
(Squamata: Colubridae: Natricinae) from Guangdong Province, China. Zootaxa 3646(3):
289-296. https://doi.org/10.11646/zootaxa.3646.3.7

Yang JH, Wang YY, Zhang B, Lau MWN, Chou WH (2011) Revision of the diagnostic charac-
ters of Opisthotropis maculosa Stuart and Chuaynkern, 2007 with notes on its distribution
and variation, and a key to the genus Opisthotropis (Squamata: Natricidae). Zootaxa 2785:
61-68. https://doi.org/10.11646/zootaxa.2785.1.4

Zhao EM (1999) Diagnoses of a new frog and a new snake from China. Sichuan Journal of
Zoology 18(3): 183.

New national record and a new species of Opisthotropis from China 159

Zhao EM, Jiang YM, Huang QY (1978) Three new snake species in China. Material for Her-
petological Researches 4: 21.

Ziegler T, David P, Thana VN (2008) A new natricine snake of the genus Opisthotropis from
Tam Dao, Vinh Phuc Province, northern Vietnam (Squamata, Colubridae). Zoosystemat-
ics and Evolution 84(2): 197-203. https://doi.org/10.1002/zoos.200800004

Ziegler T, Pham CT, Nguyen TV, Nguyen TQ, Wang J, Wang YY, Stuart BL, Le MD (2019) A
new species of Opisthotropis from northern Vietnam previously misidentified as the Yellow-
spotted Mountain Stream Keelback O. maculosa Stuart & Chuaynkern, 2007 (Squamata:
Natricidae). Zootaxa 4613(3): 579-586. https://doi.org/10.11646/zootaxa.4613.3.9